Rapid adjustment in chrysanthemum carbohydrate turnover and growth activity to a change in time-of-day application of light and daylength
Katrine Heinsvig Kjaer A E , Richard Poiré B C , Carl-Otto Ottosen A and Achim Walter B D
+ Author Affiliations
- Author Affiliations
A Department of Food Science, Aarhus University, Kirstinebjergvej 10, 5792 Aarslev, Denmark.
B IBG-2 (Plant Sciences), Forschungszentrum Jülich, 52425 Jülich, Germany.
C Present address: CSIRO Plant Industry, High Resolution Plant Phenomics Centre, Clunies Ross St, Black Mountain, 2601 ACT, Australia.
D Present address: Institute of Plant Science, ETH Zürich, 8092 Zürich, Switzerland.
E Corresponding author. Email: katrine.kjaer@agrsci.dk
Functional Plant Biology 39(8) 639-649 https://doi.org/10.1071/FP11289
Submitted: 21 December 2011 Accepted: 27 June 2012 Published: 7 August 2012
Abstract
Diel (24 h) rhythms are believed to be of great importance to plant growth and carbohydrate metabolism in fluctuating environments. However, it is unclear how plants that have evolved to experience regular day–night patterns will respond to irregular light environments that disturb diurnally-regulated parameters related to growth. In this study, chrysanthemum plants were exposed to a change in the time-of-day application of light followed by short days or long days with a night interruption of light. We observed a clear shift in the diel cycle of sucrose turnover and relative leaf expansion, indicating a resetting of these activities with a temporal trigger in the early morning. The starch pool was relatively stable in long-day plants and marginally affected by the change in the time-of-day application in light followed by long days with a night interruption. This was in contrast with an onset of a daily starch turnover by a shift to short days. These results confirm findings from model species on the complex relationship between carbohydrate metabolism, source–sink relations and growth rate and they shed new light on the dynamic processes during acclimation towards altered environmental responses of plants in fluctuating environments.
Additional keywords: diurnal regulation, carbohydrate metabolism, photosynthesis, sugar sensing.
References
Ainsworth EA, Rogers A, Leakey ABD, Heady LE, Gibon Y, Stitt M, Schurr U (2006) Does elevated [CO2] alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves. Journal of Experimental Botany 58, 579–591.| Does elevated [CO2] alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves.Crossref | GoogleScholarGoogle Scholar |
Chatterton NJ, Silvius JE (1979) Photosynthate partitioning into starch in soybean leaves. 1 Effects of photoperiod vs photosynthetic period duration. Plant Physiology 64, 749–753.
| Photosynthate partitioning into starch in soybean leaves. 1 Effects of photoperiod vs photosynthetic period duration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXlsFartw%3D%3D&md5=670dd61b7a98830c4940a58eb438c16dCAS |
Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630–633.
| Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsFChtrw%3D&md5=bac25e34a647f10e239af86ef6309873CAS |
Farré EM (2012) The regulation of plant growth by the circadian clock. Plant Biology 14, 401–410.
| The regulation of plant growth by the circadian clock.Crossref | GoogleScholarGoogle Scholar |
Fondy BR, Geiger DR, Servaites JC (1989) Photosynthesis, carbohydrate metabolism, and export in Beta vulgaris L. and Phaseolus vulgaris L. during square and sinusoidal light regimes. Plant Physiology 89, 396–402.
| Photosynthesis, carbohydrate metabolism, and export in Beta vulgaris L. and Phaseolus vulgaris L. during square and sinusoidal light regimes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXktVCntrw%3D&md5=06ec23e6539824a2b23ee15c2bba27cdCAS |
Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Hohne M, Gunther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. The Plant Journal 39, 847–862.
| Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpt1GntLo%3D&md5=3421949fbcd7cdb46018e062f808e661CAS |
Gibon Y, Pyl ET, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant, Cell & Environment 32, 859–874.
| Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2jsLY%3D&md5=f045f8b72bd70ab50c26b5f56b9daa4eCAS |
Graf A, Smith AM (2011) Starch and the clock: the dark side of plant productivity. Trends in Plant Science 16, 169–175.
| Starch and the clock: the dark side of plant productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtFCls70%3D&md5=8da1a76ea5aa535c7a293cad3a423633CAS |
Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis at night. Proceedings of the National Academy of Sciences of the United States of America 107, 9458–9463.
| Circadian control of carbohydrate availability for growth in Arabidopsis at night.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmslams70%3D&md5=4cc304f8034d58860b428203ab0dc984CAS |
Granier C, Tardieu F (1999) Leaf expansion and cell division are affected by reducing absorbed light before but not after the decline in cell division rate in the sunflower leaf. Plant, Cell & Environment 22, 1365–1376.
| Leaf expansion and cell division are affected by reducing absorbed light before but not after the decline in cell division rate in the sunflower leaf.Crossref | GoogleScholarGoogle Scholar |
Harmer SL, Hogenesch LB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110–2113.
| Orchestrated transcription of key pathways in Arabidopsis by the circadian clock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptVyisrw%3D&md5=cf4fe496bf6b2e27643d684497654c21CAS |
Jackson SD (2009) Plant responses to photoperiod. New Phytologist 60, 379–383.
Kjaer KH, Ottosen CO (2011) Growth of chrysanthemum in response to supplemental light provided by irregular light breaks during the night. Journal of the American Society for Horticultural Science 136, 3–9.
Kjaer KH, Ottosen CO, Jørgensen BN (2012) Timing growth and development of Campanula by daily light integral and supplemental light level in a cost-efficient light control system. Scientia Horticulturae 143, 189–196.
| Timing growth and development of Campanula by daily light integral and supplemental light level in a cost-efficient light control system.Crossref | GoogleScholarGoogle Scholar |
Kreps JA, Kay SA (1997) Coordination of plant metabolism and development by the circadian clock. The Plant Cell 9, 1235–1244.
| Coordination of plant metabolism and development by the circadian clock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlt1Shur4%3D&md5=86b2e7c227caa88f12b630cd1526afffCAS |
Lorenzen JH, Ewing EE (1991) Starch accumulation in leaves of potato (Solanum tuberosum L.) during the first 18 days of photoperiod treatment. Annals of Botany 69, 481–485.
Lu Y, Gehan JP, Sharkey TD (2005) Day length and circadian effects on starch degradation and maltose metabolism. Plant Physiology 138, 2280–2291.
| Day length and circadian effects on starch degradation and maltose metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXps12lsbY%3D&md5=8f0c4083ea0d47c1fab9af6dd63b105eCAS |
Matheson NK, Wheatley JM (1962) Starch changes in developing and senescing tobacco leaves. Australian Journal of Biological Sciences 15, 445–458.
Matt P, Schurr U, Klein D, Krapp A, Stitt M (1998) Growth of tobacco in short-day conditions leads to high starch, low sugars, altered diurnal changes in the Nia transcript and low nitrate reductase activity, and inhibition of amino acid synthesis. Planta 207, 27–41.
| Growth of tobacco in short-day conditions leads to high starch, low sugars, altered diurnal changes in the Nia transcript and low nitrate reductase activity, and inhibition of amino acid synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFKht74%3D&md5=0dc1c78b94e50406b8eabf96ca9e6833CAS |
McCormick AJ, Cramer MD, Watt DA (2008) Regulation of photosynthesis by sugars in sugarcane leaves. Journal of Plant Physiology 165, 1817–1829.
| Regulation of photosynthesis by sugars in sugarcane leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVKgurbL&md5=c5cd4b4591c71d0b7b2dc967b013911fCAS |
Nagel KA, Schurr U, Walter A (2006) Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity. Plant, Cell & Environment 29, 1936–1945.
| Dynamics of root growth stimulation in Nicotiana tabacum in increasing light intensity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1aktLjJ&md5=d4f9e95a0060dab2bd2c8fd2dde0271bCAS |
Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN (2007) Rhythmic growth explained by coincidence between internal and external cues. Nature 448, 358–361.
| Rhythmic growth explained by coincidence between internal and external cues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvVeqsLY%3D&md5=0dc8c6fdabeb1046edc858c9fabac59eCAS |
Nusinow DM, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011) The ELF4–ELF3-LUX complex links the circadian clock to diurnal growth of hypocotyl growth. Nature 475, 398–402.
| The ELF4–ELF3-LUX complex links the circadian clock to diurnal growth of hypocotyl growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXoslymtLk%3D&md5=56ce73847f645d0612764199b374fba8CAS |
Pantin F, Simonneau T, Rolland G, Dauzat M, Muller B (2011) Control of leaf expansion: a developmental switch from metabolics to hydraulics. Plant Physiology 156, 803–815.
| Control of leaf expansion: a developmental switch from metabolics to hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrtrs%3D&md5=061635f929b0ff666fa97c1716163001CAS |
Poiré R, Wiese-Klinkenberg A, Parent B, Mielewczik M, Schurr U, Tardieu F, Walter A (2010) Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects. Journal of Experimental Botany 61, 1751–1759.
| Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects.Crossref | GoogleScholarGoogle Scholar |
Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Australian Journal of Plant Physiology 27, 595–607.
| The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlslars7w%3D&md5=23574d12783d350a7ce3a10dcc91be3dCAS |
Ruts T, Matsubara S, Wiese-Klinkenberg A, Walter A (2012) Diel patterns of leaf and root growth: endogenous rhythmicity or environmental response. Journal of Experimental Botany 63, 3339–3351.
| Diel patterns of leaf and root growth: endogenous rhythmicity or environmental response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVSit7g%3D&md5=de955f005e7c666761ded9aa5cada6b0CAS |
Schmundt D, Stitt M, Jahne B, Schurr U (1998) Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis. The Plant Journal 16, 505–514.
| Quantitative analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis.Crossref | GoogleScholarGoogle Scholar |
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant, Cell & Environment 30, 1126–1149.
| Coordination of carbon supply and plant growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiurrJ&md5=6ef45198ede904a8f335ac52f680c1e8CAS |
Stitt M (1990) Fructose-2,6-bisphosphate as a regulatory molecule in plants. Annual Review of Plant Physiology and Plant Molecular Biology 41, 153–185.
| Fructose-2,6-bisphosphate as a regulatory molecule in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXksFGkurk%3D&md5=f07f283783076e11a13c264cc64ce39bCAS |
Stitt M, Gibon Y, Lunn JE, Piques M (2007) Multilevel genomics analysis of carbon signaling during low carbon availability: coordinating the supply and utilization of carbon in a fluctuating environment. Functional Plant Biology 34, 526–549.
| Multilevel genomics analysis of carbon signaling during low carbon availability: coordinating the supply and utilization of carbon in a fluctuating environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtVSksrY%3D&md5=a3d6de255b32220df299d1b6c9b413faCAS |
Vriet C, Welham T, Brachmann A, Pike M, Pike J, Perry J, Parniske M, Sato S, Tabata S, Smith AM, Wang TL (2010) A suite of Lotus japonicus starch mutants reveals both conserved and novel features of starch metabolism. Plant Physiology 154, 643–655.
| A suite of Lotus japonicus starch mutants reveals both conserved and novel features of starch metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCkt7vJ&md5=64a29ba104f5cf0f79fc3ac69d4ed051CAS |
Walter A (2009) Leaf growth dynamics. Nova Acta Leopoldina 357, 123–134.
Walter A, Feil R, Schurr U (2002) Restriction of nyctinastic movements and application of tensile forces to leaves affects diurnal patterns of expansion growth. Functional Plant Biology 29, 1247–1258.
| Restriction of nyctinastic movements and application of tensile forces to leaves affects diurnal patterns of expansion growth.Crossref | GoogleScholarGoogle Scholar |
Walter A, Scharr H, Gilmer F, Zierer R, Nagel KA, Ernst M, Wiese A, Virnich O, Christ MM, Uhlig B, Jünger S, Schurr U (2007) Dynamics of seedling growth acclimation towards altered light conditions can be quantified via GROWSCREEN: a setup and procedure designed for rapid optical phenotyping of different plant species. New Phytologist 174, 447–455.
| Dynamics of seedling growth acclimation towards altered light conditions can be quantified via GROWSCREEN: a setup and procedure designed for rapid optical phenotyping of different plant species.Crossref | GoogleScholarGoogle Scholar |
Walter A, Silk WK, Schurr U (2009) Environmental effects on spatial and temporal patterns of leaf and root growth. Annual Review of Plant Biology 60, 279–304.
| Environmental effects on spatial and temporal patterns of leaf and root growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFGls7c%3D&md5=2d08d916e55e46b25464b27d65d19c38CAS |
Wiese A, Christ MM, Virnich O, Schurr U, Walter A (2007) Spatio-temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle. New Phytologist 174, 752–761.
| Spatio-temporal leaf growth patterns of Arabidopsis thaliana and evidence for sugar control of the diel leaf growth cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1amtL8%3D&md5=31557f3a8f914af45b6e1b4698a1a059CAS |
